Abstract
Black light traps were used to measure the seasonal and geographical distribution of Culicoides spp. (biting midges or no-see-ums) at 9 cowsheds in the southern half of the Republic of Korea (ROK) from June through October 2010. A total of 25,242 Culicoides females (24,852; 98.5%) and males (390; 1.5%) comprising of 9 species were collected. The most commonly collected species was Culicoides punctatus (73.0%) followed by C. arakawae (25.7%), while the remaining 7 species accounted for <1.0% of all Culicoides spp. collected. The mean number of Culicoides spp. collected per trap night (Trap Index [TI]) was highest for C. punctatus (409.3), followed by C. arakawae (144.2), C. tainanus (4.1), C. oxystoma (1.2), C. circumscriptus (0.7), C. homotomus (0.6), C. erairai (0.4), C. kibunensis (0.3), and C. nipponensis (0.04). Peak TIs were observed for C. punctatus (1,188.7) and C. arakawae (539.0) during July and August, respectively. C. punctatus and C. arakawae have been implicated in the transmission of arboviruses and other pathogens of veterinary importance that adversely impact on animal and bird husbandry.
-
Key words: Culicoides punctatus, Culicoides arakawae, biting midge, seasonal abundance
INTRODUCTION
Members of the genus
Culicoides Latreille (Diptera: Ceratopogonidae), often referred to as biting midges or no-see-ums, are small (0.5-2.0 mm in length) bloodsucking insects of medical and veterinary importance [
1].
Culicoides spp. have a broad distribution and impact on human and veterinary health as vectors of viruses (e.g., bluetongue virus, African horse sickness, epizootic hemorrhagic disease of deer, Akabane, Aino, Chuzan, and bovine ephemeral fever), protozoan parasites (e.g.
Haemoproteus spp. and
Leucocytozoon spp.), and filarial worms (e.g.,
Onchocerca spp. and
Dipetalonema spp.) throughout their range [
2-
10]. In addition, the bites of
Culicoides often result in extreme annoyance, itching, lesions, and secondary infections that impact on both animal and human health [
11,
12].
The majority of
Culicoides spp. records from the Republic of Korea (ROK) were made by foreign researchers from 1918 to 1960 [
13-
19], with the first nationwide surveys of
Culicoides spp. reported in the 1970s [
20,
21]. Currently, 28 described species of
Culicoides are reported from the ROK [
21]. Of these,
C. arakawae (Arakawa),
C. oxystoma Kieffer,
C. pulicaris (L.),
C. actoni Smith, and
C. obsoletus (Meigen) have been implicated in the transmission of domestic livestock pathogens [
9,
22-
24].
More recently, Kang and Yu [
25] reported on the seasonal abundance and host blood meal analysis of
Culicoides spp. collected from cattle and poultry farms in Gyeonggi Province. Lee [
26] conducted ecological surveys that provided information on the host-seeking activity, host preferences, and seasonal and geographical distributions of
Culicoides spp. at Incheon Metropolitan City and 12 other localities from 1992-1993. Since 1993, there have been no ecological or epidemiological surveys for
Culicoides spp. reported in the ROK, even though they transmit pathogens of veterinary importance in the ROK [
10].
As part of the vector-borne disease surveillance, the Entomology Section, 5th Medical Detachment (MED DET), 168th Multifunctional Medical Battalion, 65th Medical Brigade, in coordination with Kosin University conducted monthly surveys to determine the species composition and seasonal and geographical distributions for Culicoides spp. collected at black light traps at cowsheds in the southern part of the ROK.
MATERIALS AND METHODS
Black light traps (model 'Black Hole' by BioTrap,
http://www.bio-trap.com), equipped with fine mesh screen nets and two 4-watt black light bulbs as the attractant and dependent upon local electrical sources, were used for surveillance of
Culicoides spp. at 9 cowsheds distributed throughout Jeongeup (126° 50' 50.60" E, 35° 06' 26.88" N) in Jeollabuk-do (Province), Damyang (126° 59' 13.94" E, 35° 20' 25.45" N) and Gurye (127° 27' 20.74" E, 35° 12' 10.80" N) in Jeollanam-do, Yeongcheon (128° 52' 18.95" E, 36° 10' 30.94" N) and Gunwi (128° 44' 08.37" E, 36° 09' 58.56" N) in Gyeongsangbuk-do, Jinju (128° 06' 02.28" E, 35° 06' 26.88" N), Changnyeong (128° 26' 33.57" E, 35° 31' 17.67" N) and Yangsan (129° 02' 53.12" E, 35° 25' 11.95" N) in Gyeongsangnam-do, and Ulju (129° 10' 22.72" E, 35° 39' 21.11" N) in Ulsan Metropolitan City in the southern part of the ROK (
Fig. 1). Black light traps were placed 1.5 m above the ground and operated for one night each month (June-October) from 06:00 p.m. to 08:00 a.m. the following day at each of the 9 cowsheds. Specimens were collected the following morning after each trap night, trap contents transported on dry ice to the 5th MED DET, and
Culicoides spp. separated and identified using the keys of Arnaud [
18] and the checklist of Cho and Chong [
21]. Voucher specimens are lodged in the Australian Quarantine and Inspection Service Northern Territory (AQISNT) collection, Darwin, Northern Territory, Australia.
RESULTS
A total of 25,242
Culicoides females (24,852; 98.5%) and males (390; 1.5%) comprising 9 species were collected. The most commonly collected species was
Culicoides punctatus (Meigen) (73.0%), followed by
C. arakawae (25.7%),
C. tainanus Kieffer (0.73%),
C. oxystoma (0.21%),
C. circumscriptus Kieffer (0.13%),
C. homotomus Kieffer (0.11%),
C. erairai Kono and Takahashi (0.06%),
C. kibunensis Tokunaga (0.06%), and
C. nipponensis Tokunaga (<0.01%) (
Table 1).
C. punctatus was the most frequently collected species at Yangsan and Yeongcheon, and these sites accounted for 53.2% and 35.9% of all
C. punctatus collected, respectively.
C. arakawae was the most frequently collected species at Yeongcheon (Gyeongsangbuk-do), Jinju (Gyeongsangnam-do), Gurye (Jeollanam-do), and Changnyeong (Gyeongsangnam-do) and accounted for 67.8%, 11.4%, 9.4%, and 7.4% of all
C. arakawae collected at these sites, respectively.
Monthly and total trap indices (TIs) (mean number of
Culicoides spp. collected/trap night) are shown in
Table 2. Overall TIs were highest for
C. punctatus (409.3), followed by
C. arakawae (144.2),
C. tainanus (4.1),
C. oxystoma (1.2),
C. circumscriptus (0.7),
C. homotomus (0.6),
C. erairai (0.4),
C. kibunensis (0.3), and
C. nipponensis (0.04) (
Table 2). Peak populations of
C. punctatus and
C. arakawae were observed during July (TI=1,188.7) and August (539.0), respectively (
Table 2).
The relative proportion of
C. punctatus,
C. arakawae, and other
Culicoides spp. for each site surveyed is shown in
Fig. 1. Geographically, collections with the highest proportions of
C. punctatus were observed at Yangsan (98.6%), Ulju (94.2%), and Jeongeup (73.8%), Yeongcheon (59.3), while at the other surveillance sites the proportions ranged from 17.3% to 48.1%, with the lowest proportions observed at Damyang (19.3%) and Gurye (17.3%), Jeollanam Province. Conversely, the highest proportions of
C. arakawae were observed at Damyang (76.1%) and Gurye (76.3%).
DISCUSSION
Culicoides species (biting midges) are vectors of both medical and veterinary importance, and as such, may impact on the economy of the animal industry in the ROK.
Culicoides punctatus and
C. arakawae were the primary species collected during this study and have been associated with important livestock diseases in other countries, e.g.,
Leucocytozoon cauleryi [
21] and fowl pox [
27], Fukuoka [
28], Aino, and Ibaraki viruses [
29,
30]. Consequently, surveillance of these and other species of
Culicoides and the pathogens they transmit are an important part of the veterinary health service to identify relative vector populations, their distributions, and associated pathogen infection rates (reported separately).
The dominance of
C. punctatus and
C. arakawae is similar to findings by Lee [
26], who reported that
C. punctatus,
C. arakawae, and
C. tainanus were the most commonly collected species at inland sites similar to those in our study. Whereas
C. nipponensis and
C. sinanoensis, which were not collected during our survey, were the predominant species collected from the southern coastal and eastern areas in the ROK. However, Kang and Yu [
25] found that
C. nipponensis was the dominant species (975.3/trap/night), followed by
C. punctatus (misidentified as
C. pulicaris) (73.5), and
C. arakawae (38.8) among a total of 13 species collected from a cattle farm in Gyeonggi Province. The disparity from these studies suggests that
Culicoides populations in the ROK are highly localized and extrapolations between areas must be viewed cautiously.
The dominance of
C. punctatus around cowsheds agrees with the host preference of this species for cattle [
26,
29,
30]. Although
C. arakawae appears to have a preference for feeding on birds [
31] it also readily feeds on cattle [
25,
26], which would explain its abundance around cowsheds. Further studies on
Culicoides spp. geographical and seasonal distributions, host attraction (i.e., placement of traps near human habitation and poultry, cattle, and swine farms) and biting activity, pathogen infection rates, and their role as potential vectors of zoonotic pathogens that impact on human and animal health are warranted. Although limited, these data provide a better understanding of the biology, ecology, and environmental parameters that affect relative population abundance of
Culicoides spp. that can be used to predict potential human and animal health risks and develop and implement mitigation strategies.
ACKNOWLEDGMENTS
We thank Hyun-Doo Kim, and Joo-Oh Kang, Kosin University, for their assistance in conducting Culicoides collections. We also thank Dr. Joel Gaydos, Armed Forces Health Surveillance Center, Global Emerging Infections Surveillance and Response System (AFHSC-GEIS), Silver Spring, Maryland, USA, for his administrative and technical support. This work was supported, as part of the Japanese encephalitis and malaria surveillance programs, through the joint partnership between the Uniformed Services University, Bethesda, Maryland, USA, the AFHSC-GEIS, Silver Spring, Maryland, USA, the National Center for Medical Intelligence, and the 65th Medical Brigade, ROK. The views expressed are those of the authors and should not be construed to represent the positions of the US Department of the Army or Department of Defense.
References
- 1. Howarth FG. Biosystematics of the Culicoides of Laos (Diptera: Ceratopogonidae). Int J Entomol 1985;27:1-96.
- 2. Linley JR, Hoch AL, Pinheiro FP. Biting midges (Diptera: Ceratopogonidae) and human health. J Med Entomol 1983;20:347-364.
- 3. Linley JR. Biting midges (Diptera: Ceratopogonidae) as vectors of non-viral animal pathogens. J Med Entomol 1985;22:589-599.
- 4. Kramer WL, Jones RH, Holbrook FR, Walton TE, Calisher CH. Isolation of arboviruses from Culicoides midges (Diptera: Culicidae) in Colorado during an epizootic of vesicular stomatitis New Jersey. J Med Entomol 1990;27:487-493.
- 5. Goto Y, Yamaguchi O, Kubo M. Epidemiological observations on bluetongue in sheep and cattle in Japan. Vet Ital 2004;40:78-82.
- 6. Venter GJ, Koekemoer JJ, Paweska JT. Investigations on outbreaks of African horse sickness in the surveillance zone in South Africa. Rev Sci Tech 2006;25:1097-1109.
- 7. Forman S, Hungerford N, Yamakawa M, Yanase T, Tsai HJ, Joo YS, Yang DK, Nha JJ. Climatic change impacts and risks for animal health in Asia. Rev Sci Tech 2008;27:581-597.
- 8. Purse BV, Brown HE, Harrup L, Mertens PP, Rogers DJ. Invasion of bluetongue and other orbivirus infections into Europe: the role of biological and climatic processes. Rev Sci Tech 2008;27:427-442.
- 9. Carpenter S, Wilson A, Mellor PS. Culicoides and the emergence of bluetongue virus in northern Europe. Trends Microbiol 2009;17:172-178.
- 10. Shin YK, Oem JK, Yoon S, Hyun BH, Cho IS, Yoon SS, Song JY. Monitoring of five bovine arboviral diseases transmitted by arthropod vectors in Korea. J Bacteriol Virol 2009;39:353-362.
- 11. Linley JR, Davies JB. Sandflies and tourism in Florida and the Bahamas and Caribbean area. J Econ Entomol 1971;64:264-278.
- 12. Anderson GS, Belton P, Kleider N. The hypersensitivity of horses to Culicoides bites in British Columbia. Can Vet J 1988;29:718-723.
- 13. Kinoshita S. Chosen-san Kyuketsusei Culicoides in tsukite. Dobutsugaku Zasshi 1918;30:155-160.
- 14. Tokunaga M. Medical Entomology. Part II. 1943, Tokyo, Japan. Kanahara Company. pp 853-931 (in Japanese).
- 15. Tokunaga M. Notes on biting midges from Japan and Korea (Heleidae or Ceratopogonidae, Diptera). 1955, Kyoto, Japan. Contrib Entomol Lab, Saikyo University. pp 1-8.
- 16. Barnett HC, Toshioka S. The bloodsucking insects, mites and ticks of Korea and their relation to disease transmission. 1951, San Francisco. 406th Medical General Lab.. pp 1-25.
- 17. Okanda T. Notes on some biting midges of Inner Mongolia, North China, Manchuria and Korea (Diptera, Heleidae). Jap J Sanit Zool 1954;15:131-135.
- 18. Arnaud P. The heleid genus Culicoides in Japan, Korea and Ryukyu Island (Insecta: Diptera). Microentomol 1956;21:84-207.
- 19. Bullock HR, Akiyama J. A new biting midge from Japan and Korea (Diptera, Heleidae). Jap J Sanit Zool 1959;10:1-25.
- 20. Cho HC, Chong CS, Yu HS. Notes on biting midges of the Culicoides from South Korea. Rep. 1972, Yongsan, Korea. 5th Preventive Medicine Unit, 8th US Army. pp 1-64.
- 21. Cho HC, Chong CS. Notes on biting midges of the Culicoides from South Korea, with special reference to unrecorded species and distribution. Korean J Parasitol 1974;12:45-75.
- 22. Akiba K. Studies on the Leucocytozoon found in the chicken in Japan. II. On the transmission of L. caulleryi by Culicoides arakawae. J Jpn Soc Vet Sci 1960;22:309-318.
- 23. Standfast HA, Muller MJ, Dyce AL. In Walton TE, Osburn BI eds, An overview of bluetongue virus vector biology and ecology in the Oriental and Australasian regions of the Western Pacific. Bluetongue, African Horse Sickness and Related Orbiviruses: proceedings of the Second International Symposium. 1992, Paris, France. pp 253-261.
- 24. Kurogi H, Akiba K, Inaba Y, Matumoto M. Isolation of Akabane virus from the biting midge Culicoides oxystoma in Japan. Vet Microbiol 1987;15:243-248.
- 25. Kang CH, Yu HS. Seasonal abundance and host blood meal sources of the genus Culicoides (Diptera: Ceratopogonidae) from cattle and poultry farms in Kyeonggi Province, Korea. Korean J Entomol 1991;21:29-36.
- 26. Lee YJ. Ecological studies in the genus Culicoides in Korea. MS Thesis. 1993, Incheon University. pp 1-46.
- 27. Fukuda T, Goto T, Kitaoka S, Fujisaki K, Takamatsu H. Experimental transmission of fowl pox by Culicoides arakawae. Natl Inst Anim Health Q (Tokyo) 1979;19:104-105.
- 28. Kaneko N, Inaba Y, Akashi H, Miura Y, Shorthose J, Kurashige K. Isolation of a new bovine ephemeral fever group virus. Aust Vet J 1986;63:29.
- 29. Lassen SB, Nielsen SA, Skovgård H, Kristensen M. Molecular identification of bloodmeals from biting midges (Diptera: Ceratopogonidae: Culicoides Latreille) in Denmark. Parasitol Res 2011;108:823-829.
- 30. Yanase T, Kato T, Kubo T, Yoshida K, Ohashi S, Yamakawa M, Miura Y, Tsuda T. Isolation of bovine arboviruses from Culicoides biting midges (Diptera: Ceratopogonidae) in Southern Japan: 1985-2002. J Med Entomol 2005;42:63-67.
- 31. Kitaoka S, Cheah TS. Seasonal incidence and feeding preference of Culicoides species caught in chicken houses and cattle sheds at Ipoh in peninsular Malaysia (Diptera: Ceratopogonidae). Malays Vet J 1983;7:245-253.
Fig. 1Surveyed areas and relative proportion of Culicoides spp. collected by black light traps in each collection site, Republic of Korea, 2010.
Table 1.Number (%) of Culicoides spp. collected from 9 surveyed areas from June to October 2010
Table 1.
|
Species |
Jeongeup |
Damyang |
Gurye |
Gunwi |
Yeongcheon |
Ulju |
Chang- nyeong |
Yangsan |
Jinju |
Total |
|
Culicoides arakawae
|
41 (20.3) |
83 (76.1) |
612 (76.3) |
122 (52.4) |
4,399 (39.8) |
26 (4.7) |
480 (52.5) |
11 (0.1) |
717 (49.6) |
6,491 (25.7) |
|
Culicoides circumscriptus
|
0 |
0 |
0 |
3 (1.3) |
24 (0.2) |
1 (0.2) |
2 (0.2) |
0 |
2 (0.1) |
32 (0.1) |
|
Culicoides erairai
|
0 |
1 (0.9) |
0 |
0 |
7 (0.1) |
1 (0.2) |
0 |
7 (0.1) |
0 |
16 ( < 0.1) |
|
Culicoides homotomus
|
0 |
0 |
1 (0.1) |
0 |
0 |
0 |
0 |
0 |
27 (1.9) |
28 (0.1) |
|
Culicoides tainanus
|
12 (5.9) |
1 (0.9) |
3 (0.4) |
0 |
51 (0.5) |
3 (0.5) |
0 |
114 (1.1) |
1 (0.1) |
185 (0.7) |
|
Culicoides nipponensis
|
0 |
0 |
0 |
0 |
0 |
0 |
0 |
0 |
2 (0.1) |
2 ( < 0.1) |
|
Culicoides oxystoma
|
0 |
3 (2.8) |
41 (5.1) |
0 |
7 |
0 |
0 |
2 ( < 0.1) |
0 |
53 (0.2) |
|
Culicoides kibunensis
|
0 |
0 |
6 (0.7) |
0 |
6 (0.1) |
1 (0.2) |
0 |
1 ( < 0.1) |
1 (0.1) |
15 ( < 0.1) |
|
Culicoides punctatus
|
149 (73.7) |
21 (19.3) |
139 (17.3) |
108 (46.4) |
6,547 (59.3) |
520 (94.2) |
433 (47.3) |
9,807 (98.6) |
696 (48.1) |
18,420 (73.0) |
|
Total |
202 |
109 |
802 |
233 |
11,041 |
552 |
915 |
9,942 |
1,446 |
25,242 |
Table 2.Monthly trap indices of Culicoides spp. collected from black light traps at 9 collection sites (cowsheds) in the southern part of the ROK, 2010
Table 2.
|
Culicoides species |
June |
July |
August |
September |
October |
Trap Indexb
|
|
C. arakawae
|
21.0a
|
155.9 |
539.0 |
4.2 |
1.1 |
144.2 |
|
C. circumscriptus
|
0.4 |
2.4 |
0.7 |
0 |
0 |
0.7 |
|
C. erairai
|
0.2 |
0.9 |
0.7 |
0 |
0 |
0.4 |
|
C. homotomus
|
1.8 |
1.3 |
0 |
0 |
0 |
0.6 |
|
C. tainanus
|
0.1 |
3 |
14.9 |
0 |
2.6 |
4.1 |
|
C. nipponensis
|
0.1 |
0 |
0.1 |
0 |
0 |
< 0.1 |
|
C. oxystoma
|
0 |
0.4 |
5.3 |
0 |
0.1 |
1.2 |
|
C. kibunensis
|
0.4 |
0.1 |
1.1 |
0 |
0 |
0.3 |
|
C. punctatus
|
114.4 |
1,188.7 |
622.8 |
75.7 |
45.1 |
409.3 |
|
Total |
138.4 |
1,352.7 |
1,184.6 |
79.9 |
48.9 |
560.8 |
